Double dissociation of neural responses supporting perceptual and cognitive components of social cognition: evidence from processing of others' pain

Abstract

Models on how perceptual and cognitive information on others' mental states are treated by the cognitive architecture are often framed as duplex models considering two independent systems. In the context of the neuroscience of empathy analogous systems have been described. Using event-related potentials (i.e., ERPs) technique, we tested the hypothesis of temporal dissociation of two functional systems. We implemented a design in which perceptual (i.e., painful or neutral facial expressions) and contextual (i.e., painful or neutral related sentences) cues on others' mental states were orthogonally manipulated. Painful expressions selectively modulated the early activity at 110-360 ms over fronto-central and centro-parietal regions, whereas painful contexts selectively modulated the late activity at 400-840 ms over these same regions. Notably, the reactions to pain triggered by these cues added up when both were available, that is the joint reaction was characterized by additive effects. These findings favor a model assuming distinct neural paths of perceptual and cognitive processing, at least when the cognitive component is triggered by language.

Figure 1. Timeline and conditions in the present experiment.

Figure 2

(a) Bar charts displaying mean accuracy and mean RT for each experimental conditions and (b) bar charts of mean rating scores for each condition. Error bars represent standard errors. Colors of the bars relate to colors of the ERP waveforms for corresponding conditions.

Figure 3

(a) Grand averages of the face-locked ERP waveforms recorded at pooled fronto-central electrode sites for each experimental condition in comparison to the neutral condition (in black color). The perception-based reaction (i.e., reactions to painful facial expressions that were preceded by neutral contexts; in blue color) selectively involved the earlier portion of the ERP waveforms (i.e., P2 and N2−N3 components), which were significantly more positive in response to painful relative to neutral facial expressions. The context-based reaction (i.e., reactions to neutral faces preceded by painful contexts; in red color) selectively interested the P3, which was significantly more positive in response to painful relative to neutral contexts. The joint reaction (i.e., reactions to painful faces preceded by painful contexts; in green color) involved the P2, N2−N3 and the P3, which were significantly more positive when both the face and the context were painful relative to the neutral condition; the joint reaction was characterized by additive effects (i.e., no interaction) of reactions triggered by perceptual and contextual cues. The figure shows also source estimation of the P2 and N2–N3 activities in the painful vs. non-painful facial expression conditions (perception-based reaction; the left anterior insula/inferior frontal gyrus and the left inferior parietal lobule/intraparietal sulcus, respectively) and the source estimation of the P3 activity in painful vs. non-painful conditions as a function of contextual information (context-based reaction; the bilateral superior frontal gyri). (b) Grand averages the face-locked ERP waveforms of all conditions superimposed recorded at pooled centro-parietal electrode sites. The N2−N3 were selectively modulated by painful facial expressions, whereas the P3 was selectively modulated by painful contexts.

Figure 4. Mean perception-based reaction, context-based reaction and joint reaction for each ERP temporal window at pooled fronto-central electrode sites (the left bar chart) and centro-parietal electrode sites (the right bar chart) computed as differential mean amplitudes between the critical condition for eliciting each reaction and the ERP elicited in the neutral condition.

Error bars represent standard errors.